Behavioral Ecology and Sociobiology

, Volume 67, Issue 3, pp 471–479 | Cite as

Denning behaviour of the European badger (Meles meles) correlates with bovine tuberculosis infection status

  • Nicola WeberEmail author
  • Stuart Bearhop
  • Sasha R. X. Dall
  • Richard J. Delahay
  • Robbie A. McDonald
  • Stephen P. Carter
Original Paper


Heterogeneities in behaviours of individuals may underpin important processes in evolutionary biology and ecology, including the spread of disease. Modelling approaches can sometimes fail to predict disease spread, which may partly be due to the number of unknown sources of variation in host behaviour. The European badger is a wildlife reservoir for bovine tuberculosis (bTB) in Britain and Ireland, and individual behaviour has been demonstrated to be an important factor in the spread of bTB among badgers and to cattle. Radio-telemetry devices were deployed on 40 badgers from eight groups to investigate patterns of den (sett) use in a high-density population, where each group had one or two main and three to eight outlier setts in their territory. Badgers were located at their setts for 28 days per season for 1 year to investigate how patterns differed between individuals. Denning behaviour may have a strong influence on contact patterns and the transmission of disease. We found significant heterogeneity, influenced by season, sex and age. Also, when controlling for these, bTB infection status interacting with season was highly correlated with sett use. Test-positive badgers spent more time away from their main sett than those that tested negative. We speculate that wider-ranging behaviour of test-positive animals may result in them contacting sources of infection more frequently and/or that their behaviour may be influenced by their disease status. Measures to control infectious diseases might be improved by targeting functional groups, specific areas or times of year that may contribute disproportionately to disease spread.


Disease transmission Movement patterns Denning behaviour Space use Wildlife disease management 



We would like to thank the Woodchester Park field team for trapping and sampling badgers, in particular P. Spyvee for additional instruction on collar fitting. We are grateful to A. Tomlinson, K. Palphramand and S. Weber for discussion, data and comments. In addition, comments from two anonymous reviewers and the Associate Editor greatly improved earlier drafts of this manuscript. This study was funded by the Department for Environment, Food and Rural Affairs (DEFRA) Project SE3032.

Ethical Standards

The experiments in this manuscript comply with the current laws of the country in which they were performed. Trapping and anaesthesia of badgers were carried out under licence from the UK Home Office (PPL60/3609) according to the Animals (Scientific Procedures) Act 1986. Procedures were approved by the Food and Environment Research Agency Ethical Review Panel.

Supplementary material

265_2012_1467_MOESM1_ESM.docx (70 kb)
ESM 1 (DOCX 69 kb)


  1. Altizer S, Nunn CL, Thrall PH, Gittleman JL, Antonovics J et al (2003) Social organization and parasite risk in mammals: integrating theory and empirical studies. Annu Rev Ecol Evol Syst 34:517–547CrossRefGoogle Scholar
  2. Barber I, Dingemanse NJ (2010) Parasitism and the evolutionary ecology of animal personality. Philos T Roy Soc B 365:4077–4088CrossRefGoogle Scholar
  3. Barlow ND (2001) Non-linear transmission and simple models for bovine tuberculosis. J Anim Ecol 69:703–713CrossRefGoogle Scholar
  4. Böhm M, Palphramand KL, Newton-Cross G, Hutchings MR, White PCL (2008) Dynamic interactions among badgers: implications for sociality and disease transmission. J Anim Ecol 77:735–745PubMedCrossRefGoogle Scholar
  5. Bourne FJ (2007) Bovine TB: the scientific evidence. Final report of the Independent Scientific Group on Cattle TB. Department for Environment, Food and Rural Affairs, LondonGoogle Scholar
  6. Boyer N, Réale D, Marmet J, Pisanu B, Chapuis J-L (2010) Personality, space use and tick load in an introduced population of Siberian chipmunks Tamias sibiricus. J Anim Ecol 79:538–547PubMedCrossRefGoogle Scholar
  7. Butler JM, Roper TJ (1996) Ectoparasites and sett use in European badgers. Anim Behav 52:621–629CrossRefGoogle Scholar
  8. Caley P, Spencer NJ, Cole RA, Efford MG (1998) The effect of manipulating population density on the probability of den-sharing among common brushtail possums, and the implications for transmission of bovine tuberculosis. Wildlife Res 25:383–392CrossRefGoogle Scholar
  9. Carpenter PJ, Pope LC, Greig C, Dawson DA, Rogers LM, Erven K, Wilson GJ, Delahay RJ, Cheeseman CL, Burke T (2005) Mating system of the Eurasian badger, Meles meles, in a high density population. Mol Ecol 14:273–284PubMedCrossRefGoogle Scholar
  10. Carter SP, Delahay RJ, Smith GC, Macdonald DW, Riordan P, Etherington TR, Pimley ER, Walker NJ, Cheeseman CL (2007) Culling-induced social perturbation in Eurasian badgers Meles meles and the management of TB in cattle: an analysis of a critical problem in applied ecology. Proc R Soc Lond B 274:2769–2777CrossRefGoogle Scholar
  11. Chambers MA, Crawshaw T, Waterhouse S, Delahay R, Hewinson RG, Lyashchenko KP (2008) Validation of the BrockTB Stat-Pak assay for detection of tuberculosis in Eurasian badgers (Meles meles) and influence of disease severity on diagnostic accuracy. J Clin Microbiol 46:1498–1500PubMedCrossRefGoogle Scholar
  12. Chambers MA, Waterhouse S, Lyashchenko K, Delahay R, Sayers R, Hewinson RG (2009) Performance of TB immunodiagnostic tests in Eurasian badgers (Meles meles) of different ages and the influence of duration of infection on serological sensitivity. BMC Vet Res 5:42PubMedCrossRefGoogle Scholar
  13. Cheeseman CL, Mallinson PJ (1981) Behaviour of badgers (Meles meles) infected with bovine tuberculosis. J Zool 194:284–9CrossRefGoogle Scholar
  14. Cheeseman CL, Wilesmith JW, Stuart FA (1989) Tuberculosis: the disease and its epidemiology in the badger, a review. Epidemiol Infect 103:113–125PubMedCrossRefGoogle Scholar
  15. Clay CA, Lehmer EM, Previtali A, St. Jeor S, Dearing MD (2009) Contact heterogeneity in deer mice: implications for Sin Nombre virus transmission. Proc Roy Soc Lond B 276:1305–1312CrossRefGoogle Scholar
  16. Clements GM et al (2011) Movements of white-tailed deer in riparian habitat: implications for infectious diseases. J Wildlife Manage 75:1436–1442CrossRefGoogle Scholar
  17. Crawley MJ (2007) The R book. Wiley, ChichesterCrossRefGoogle Scholar
  18. Cross PC, Drewe J, Patrek V, Pearce G, Samuel MD, Delahay RJ (2009) Wildlife population structure and parasite transmission: implications for disease management. In: Delahay RJ, Smith GC, Hutchings MR (eds) Management of disease in wild mammals. Springer, Tokyo, pp 9–29CrossRefGoogle Scholar
  19. Dall SRX, Bel AM, Bolnick DI, Ratnieks W (2012) An evolutionary ecology of individual differences. Ecol Lett 15:1189–1198PubMedCrossRefGoogle Scholar
  20. Dalley D, Davé D, Lesellier S, Palmer S, Crawshaw T, Hewinson RG, Chambers M (2008) Development and evaluation of a gamma-interferon assay for tuberculosis in badgers (Meles meles). Tuberculosis 88:235–243PubMedCrossRefGoogle Scholar
  21. Delahay RJ, Langton S, Smith GC, Clifton-Hadley RS, Cheeseman CL (2000a) The spatio-temporal distribution of Mycobacterium bovis (bovine tuberculosis) infection in a high-density badger population. J Anim Ecol 69:428–441CrossRefGoogle Scholar
  22. Delahay RJ, Brown JA, Mallinson PJ, Spyvee PD, Handoll D, Rogers LM, Cheeseman CL (2000b) The use of marked bait in studies of the territorial organization of the European Badger (Meles meles). Mammal Rev 30:73–87CrossRefGoogle Scholar
  23. Delahay RJ, Wilson GJ, Smith GC, Cheeseman CL (2003) Vaccinating badgers (Meles meles) against Mycobacterium bovis: the ecological considerations. Vet J 166:43–51PubMedCrossRefGoogle Scholar
  24. Delahay RJ, Carter SP, Forrester GJ, Mitchell A, Cheeseman CL (2006a) Habitat correlates of group size, bodyweight and reproductive performance in a high-density Eurasian badger (Meles meles) population. J Zool 270:437–447CrossRefGoogle Scholar
  25. Delahay RJ, Walker NJ, Forrester GJ, Harmsen B, Riordan P, Macdonald DW, Newman C, Cheeseman CL (2006b) Demographic correlates of bite wounding in Eurasian badgers, Meles meles L., in stable and perturbed populations. Anim Behav 71:1047–1055CrossRefGoogle Scholar
  26. Donnelly CA, Woodroffe R, Cox DR, Bourne J, Cheeseman CL, Clifton-Hadley RS, Wei G, Gettinby G, Gilks P, Jenkins H, Johnston WT, Le Fevre AM, McInerney JP, Morrison WI (2005) Positive and negative effects of widespread badger culling on tuberculosis in cattle. Nature 439:843–846PubMedCrossRefGoogle Scholar
  27. Dugdale HL, Macdonald DW, Pope LC, Burke T (2007) Polygynandry, extra-group paternity and multiple-paternity litters in European badger (Meles meles) social groups. Mol Ecol 16:5294–5306PubMedCrossRefGoogle Scholar
  28. Dugdale HL, Ellwood SA, Macdonald DW (2010) Alloparental behaviour and long-term costs of mothers tolerating other group-members in a plurally breeding mammal. Anim Behav 80:721–735CrossRefGoogle Scholar
  29. Easterbrook JD, Kaplan JB, Glass GE, Pletnikov MV, Klein SL (2007) Elevated testosterone and reduced 5-HIAA concentrations are associated with wounding and hantavirus infection in male Norway rats. Horm Behav 52:474–481PubMedCrossRefGoogle Scholar
  30. Garnett BT, Delahay RJ, Roper TJ (2005) Ranging behaviour of European badgers (Meles meles) in relation to bovine tuberculosis (Mycobacterium bovis) infection. Appl Anim Behav Sci 94:331–340CrossRefGoogle Scholar
  31. Gascoyne SC, Laurenson MK, Lelo S, Bomer M (1993) Rabies in African wild dogs (Lycaon pictus) in the Serengeti region, Tanzania. J Wildlife Dis 29:396–402Google Scholar
  32. Harris S, Cresswell P, Jefferies D (1989) Surveying badgers. The Mammal Society, publication no. 9. Mammal Society, BristolGoogle Scholar
  33. Jackson R, de Lisle GW, Morris RS (1995) A study of the environmental survival of Mycobacterium bovis on a farm in New Zealand. New Zeal Vet J 43:346–352CrossRefGoogle Scholar
  34. Jenkins HE, Cox DR, Delahay RJ (2012) Direction of association between bite wounds and Mycobacterium bovis infection in badgers: implications for transmission. PLoS One 7:e45584PubMedCrossRefGoogle Scholar
  35. Johnson AM, Wadsworth J, Wellings K, Field J (1994) Sexual attitudes and lifestyles. Blackwell Science, OxfordGoogle Scholar
  36. Johnson DDP, Macdonald DW, Dickman AJ (2000) An analysis and review of models of the sociobiology of the Mustelidae. Mammal Rev 30:171–196CrossRefGoogle Scholar
  37. Kaneko Y, Newman C, Buesching CD, Macdonald DW (2010) Variations in badger (Meles meles) sett microclimate: differential cub survival between main and subsidiary setts, with implications for artificial sett construction. Int J Ecol 859586:10Google Scholar
  38. Kilpatrick AM, Daszak P, Jones MJ, Marra PP, Kramer LD (2006) Host heterogeneity dominates West Nile virus transmission. Proc Roy Soc Lond B 273:2327–2333CrossRefGoogle Scholar
  39. Kilpatrick AM, Gillin CM, Daszak P (2009) Wildlife–livestock conflict: the risk of pathogen transmission from bison to cattle outside Yellowstone National Park. J Appl Ecol 46:476–485CrossRefGoogle Scholar
  40. Kowalczyk R, Zalewski A, Jȩdrzejewska B (2004) Seasonal and spatial pattern of shelter use by badgers Meles meles in Białowieża Primeval Forest (Poland). Acta Theriol 49:75–92CrossRefGoogle Scholar
  41. Kruuk H (1978) Foraging and spatial organisation of the European badger, Meles meles L. Behav Ecol Sociobiol 4:75–89CrossRefGoogle Scholar
  42. Le Cren ED (1951) The length–weight relationship and seasonal cycle in gonad weight and condition in the perch (Perca fluviatilis). J Anim Ecol 20:201–219CrossRefGoogle Scholar
  43. Lloyd-Smith JO, Schreiber SJ, Kopp PE, Getz WM (2005) Superspreading and the effect of individual variation on disease emergence. Nature 438:355–359PubMedCrossRefGoogle Scholar
  44. Macdonald DW, Newman C, Dean J, Buesching CD, Johnson PJ (2004) The distribution of Eurasian badger, Meles meles, setts in a high-density area: field observations contradict the sett dispersion hypothesis. Oikos 106:295–307CrossRefGoogle Scholar
  45. McCallum H, Jones M (2006) To lose both would look like carelessness: Tasmanian devil facial tumour disease. PLoS Biol 4:e342PubMedCrossRefGoogle Scholar
  46. McGraw KO, Wong SP (1996) Forming inferences about some intraclass correlation coefficients. Psychol Methods 1:30–46CrossRefGoogle Scholar
  47. Muirhead RH, Gallagher J, Burn KJ (1974) Tuberculosis in wild badgers in Gloucestershire: epidemiology. Vet Rec 95:552–555CrossRefGoogle Scholar
  48. Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956PubMedGoogle Scholar
  49. Natoli E, Say L, Cafazzo S, Bonanni R, Schmid M, Pontier D (2005) Bold attitude makes male urban feral domestic cats more vulnerable to Feline Immunodeficiency Virus. Neurosci Biobehav R 29:151–157CrossRefGoogle Scholar
  50. Neal E, Cheeseman C (1996) Badgers. Cambridge University Press, CambridgeGoogle Scholar
  51. Neal E, Roper TJ (1991) The environmental impact of badgers (Meles meles) and their setts. Sym Zool S 63:89–106Google Scholar
  52. Perkins SE, Cattadori IM, Tagliapietra V, Rizzoli AP, Hudson PJ (2003) Empirical evidence for key hosts in persistence of a tick-borne disease. Int J Parasitol 33:909–917PubMedCrossRefGoogle Scholar
  53. R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  54. Riordan P, Delahay RJ, Cheeseman C, Johnson PJ, Macdonald DW (2011) Culling-induced changes in badger (Meles meles) behaviour, social organisation and the epidemiology of bovine tuberculosis. PLoS One 6:e28904PubMedCrossRefGoogle Scholar
  55. Rogers LM, Forrester GJ, Wilson GJ, Yarnell RW, Cheeseman CL (2003) The role of setts in badger (Meles meles) group size, breeding success and status of TB (Mycobacterium bovis). J Zool 260:209–215CrossRefGoogle Scholar
  56. Roper TJ (2010) Badger. HarperCollins, LondonGoogle Scholar
  57. Roper TJ, Ostler JR, Schmid TK, Christian SF (2001) Sett use in European badgers Meles meles. Behaviour 138:173–187CrossRefGoogle Scholar
  58. Sauter CM, Morris RS (1995) Behavioural studies on the potential for direct transmission of tuberculosis from feral ferrets (Mustelo furo) and possums (Trichosurus vulpecula) to farmed livestock. New Zeal Vet J 43:294–300CrossRefGoogle Scholar
  59. Shen Z, Ning F, Zhou W, He X, Lin C, Chin DP, Zhu Z, Schuchat A (2004) Superspreading SARS events, Beijing 2003. Emerg Infect Dis 10:256–260PubMedCrossRefGoogle Scholar
  60. Sin YW, Dugdale HL, Newman C, Macdonald DW, Burke T (2012) MHC class II in the European badger (Meles meles): characterization, patterns of variation, and transcription analysis. Immunogenetics 64:313–327PubMedCrossRefGoogle Scholar
  61. Skorping A, Jensen KH (2004) Disease dynamics: all caused by males? Trends Ecol Evol 19:219–220PubMedCrossRefGoogle Scholar
  62. Smith GC, Richards MS, Clifton-Hadley RS, Cheeseman CL (1995) Modelling bovine tuberculosis in badgers in England: preliminary results. Mammalia 59:639–50Google Scholar
  63. Soper GA (1939) The curious career of typhoid Mary. B New York Acad Med 15:698–712Google Scholar
  64. Stewart PD, Macdonald DW (2003) Badgers and badger fleas: strategies and counter-strategies. Ethology 109:751–764CrossRefGoogle Scholar
  65. Vicente J, Delahay RJ, Walker N, Cheeseman CL (2007) Social organization and movement influence the incidence of bovine tuberculosis in an undisturbed high density badger Meles meles population. J Anim Ecol 76:348–360PubMedCrossRefGoogle Scholar
  66. Woelfing B, Traulsen A, Milinski M, Boehm T (2009) Does intra-individual major histocompatibility complex diversity keep a golden mean? Proc Roy Soc Lond B 364:117–128Google Scholar
  67. Woodroffe R (1993) Alloparental behaviour in the European badger. Anim Behav 46:413–415CrossRefGoogle Scholar
  68. Woodroffe R, Macdonald DW (2000) Helpers provide no detectable benefits in the European badger (Meles meles). J Zool 250:113–119CrossRefGoogle Scholar
  69. Woodroffe R, Frost SDW, Clifton-Hadley RS (1999) Attempts to control tuberculosis in cattle by removing infected badgers: constraints imposed by live test sensitivity. J Appl Ecol 36:494–501CrossRefGoogle Scholar
  70. Woodroffe R, Donnelly CA, Johnston WT, Bourne FJ, Cheeseman CL, Clifton-Hadley RS, Cox DR, Gettinby G, Hewinson RG, Le Fevre AM, McInerney JP, Morrison WI (2005a) Spatial association of Mycobacterium bovis infection in cattle and badgers Meles meles. J Appl Ecol 42:852–862CrossRefGoogle Scholar
  71. Woodroffe R, Bourne FJ, Cheeseman CI, Cox DR, Donnelly CA, Gettinby G, McInerney JP, Morrison WI (2005b) Welfare of badgers (Meles meles) subjected to culling: development and evaluation of a closed season. Anim Welfare 14:19–25Google Scholar
  72. Woolhouse MEJ, Dye C, Etard J-F, Smith T, Charlwood JD et al (1997) Heterogeneities in the transmission of infectious agents: implications for the design of control programs. P Natl Acad Sci USA 94:338–342CrossRefGoogle Scholar
  73. Zuk M, McKean KA (1996) Sex differences in parasite infections: patterns and processes. Int J Parasitol 26:1009–1024PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Nicola Weber
    • 1
    • 2
    Email author
  • Stuart Bearhop
    • 1
  • Sasha R. X. Dall
    • 1
  • Richard J. Delahay
    • 2
  • Robbie A. McDonald
    • 3
  • Stephen P. Carter
    • 2
  1. 1.Centre for Ecology and Conservation, College of Life & Environmental SciencesUniversity of ExeterPenrynUK
  2. 2.The Food and Environment Research AgencyYorkUK
  3. 3.Environment and Sustainability Institute, College of Life & Environmental SciencesUniversity of ExeterPenrynUK

Personalised recommendations